Retinoic acid metabolism and signaling pathways in the adult and developing mouse testis

Endocrinology

Volumn 147, Issue 1, 2006, Pages 96-110

  Vernet, Nadège ^a   Dennefeld, Christine ^a   Rochette Egly, Cécile ^a   Oulad Abdelghani, Mustapha ^a   Chambon, Pierre ^a   Ghyselinck, Norbert B ^a   Mark, Manuel ^a,b  

^a CNRS   (France)

^b INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME P450; FAT DROPLET; HETERODIMER; OXYGENASE; PHOSPHATIDYLCHOLINE; RECEPTOR; RECEPTOR SUBUNIT; RETINOIC ACID; RETINOIC ACID RECEPTOR; RETINOIC ACID RECEPTOR BETA; RETINOL ACYLTRANSFERASE; REXINOID RECEPTOR; REXINOID RECEPTOR ALPHA; REXINOID RECEPTOR GAMMA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CATABOLISM; CELL COMPARTMENTALIZATION; CELL PROLIFERATION; CONTROLLED STUDY; GENE MUTATION; LEYDIG CELL; MALE; MOUSE; NONHUMAN; PARACRINE SIGNALING; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RETINOL DEFICIENCY; SEMINIFEROUS TUBULE EPITHELIUM; SERTOLI CELL; SIGNAL TRANSDUCTION; SPERMATID; SPERMATOGENESIS; SPERMATOGONIUM; TESTIS DEVELOPMENT;

ANIMALS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MICE; RECEPTORS, RETINOIC ACID; SIGNAL TRANSDUCTION; TESTIS; TRETINOIN;

EID: 29444444570     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2005-0953     Document Type: Article

References (82)

1. Wolbach SB, Howe PR 1925 Tissue changes following deprivation of fat-soluble A vitamin. J Exp Med 42:753-777
2. Ghyselinck NB, Bavik C, Sapin V, Mark M, Bonnier D, Hindelang C, Dierich A, Nilsson CB, Hakansson H, Sauvant P, Azais-Braesco V, Frasson M, Picaud S, Chambon P 1999 Cellular retinol-binding protein I is essential for vitamin A homeostasis. EMBO J 18:4903-4914
3. Appling DR, Chytil F 1981 Evidence of a role for retinoic acid (vitamin A-acid) in the maintenance of testosterone production in male rats. Endocrinology 108:2120-2124
4. Huang HF, Dyrenfurth I, Hembree WC 1983 Endocrine changes associated with germ cell loss during vitamin A-induced recovery of spermatogenesis. Endocrinology 112:1163-1171
5. Morales A, Cavicchia JC 2002 Spermatogenesis and blood-testis barrier in rats after long-term vitamin A deprivation. Tissue Cell 34:349-355
6. Huang HF, Marshall GR 1983 Failure of spermatid release under various vitamin A states: an indication of delayed spermiation. Biol Reprod 28:1163-1172
7. Griswold MD, Bishop PD, Kim KH, Ping R, Siiteri JE, Morales C 1989 Function of vitamin A in normal and synchronized seminiferous tubules. Ann NY Acad Sci 564:154-172
8. van Pelt AM, de Rooij DG 1991 Retinoic acid is able to reinitiate spermatogenesis in vitamin A-deficient rats and high replicate doses support the full development of spermatogenic cells. Endocrinology 128:697-704
9. Kurlandsky SB, Gamble MV, Ramakrishnan R, Blaner WS 1995 Plasma delivery of retinoic acid to tissues in the rat. J Biol Chem 270:17850-17857
10. Schmidt CK, Brouwer A, Nau H 2003 Chromatographic analysis of endogenous retinoids in tissues and serum. Anal Biochem 315:36-48
11. Duester G 2001 Genetic dissection of retinoid dehydrogenases. Chem Biol Interact 130-132:469-480
12. Soprano DR, Blaner WS 1994 Plasma retinol-binding protein. In: Sporn MB, Roberts AB, Goodman DS, eds. The retinoids: biology, chemistry and medicine. 2nd ed. New York: Raven Press; 257-281
13. Ross AC 2003 Retinoid production and catabolism: role of diet in regulating retinol esterification and retinoic acid oxidation. J Nutr 133:291S-296S
14. Deltour L, Haselbeck RJ, Ang HL, Duester G 1997 Localization of class I and class IV alcohol dehydrogenases in mouse testis and epididymis: potential retinol dehydrogenases for endogenous retinoic acid synthesis. Biol Reprod 56:102-109
15. Molotkov A, Fan X, Deltour L, Foglio MH, Martras S, Farres J, Pares X, Duester G 2002 Stimulation of retinoic acid production and growth by ubiquitously expressed alcohol dehydrogenase Adh3. Proc Natl Acad Sci USA 99:5337-5342
16. Lin M, Zhang M, Abraham M, Smith SM, Napoli JL 2003 Mouse retinal dehydrogenase 4 (RALDH4), molecular cloning, cellular expression, and activity in 9-cis-retinoic acid biosynthesis in intact cells. J Biol Chem 278:9856-9861
17. Zhai Y, Sperkova Z, Napoli JL 2001 Cellular expression of retinal dehydrogenase types 1 and 2: effects of vitamin A status on testis mRNA. J Cell Physiol 186:220-232
18. Lopez-Fernandez LA, del Mazo J 1997 The cytosolic aldehyde dehydrogenase gene (Aldh1) is developmentally expressed in Leydig cells. FEBS Lett 407:225-229
19. Napoli JL, Race KR 1988 Biogenesis of retinoic acid from β-carotene. Differences between the metabolism of β-carotene and retinal. J Biol Chem 263:17372-17377
20. Paik J, During A, Harrison EH, Mendelsohn CL, Lai K, Blaner WS 2001 Expression and characterization of a murine enzyme able to cleave β-carotene. The formation of retinoids. J Biol Chem 276:32160-32168
21. Niederreither K, Abu-Abed S, Schuhbaur B, Petkovich M, Chambon P, Dolle P 2002 Genetic evidence that oxidative derivatives of retinoic acid are not involved in retinoid signalling during mouse development. Nat Genet 31:84-88
22. Taimi M, Helvig C, Wisniewski J, Ramshaw H, White J, Amad M, Korczak B, Petkovich M 2004 A novel human cytochrome P450, CYP26C1, involved in metabolism of 9-cis and all-trans isomers of retinoic acid. J Biol Chem 279:77-85
23. Napoli JL 1999 Retinoic acid: its biosynthesis and metabolism. Prog Nucleic Acids Res Mol Biol 63:139-188
24. E X, Zhang L, Lu J, Tso P, Blaner WS, Levin MS, Li E 2002 Increased neonatal mortality in mice lacking cellular retinol-binding protein II. J Biol Chem 277:36617-36623
25. Rajan N, Sung WK, Goodman DS 1990 Localization of cellular retinol-binding protein mRNA in rat testis and epididymis and its stage-dependent expression during the cycle of the seminiferous epithelium. Biol Reprod 43:835-842
26. Zhai Y, Higgins D, Napoli JL 1997 Coexpression of the mRNAs encoding retinol dehydrogenase isozymes and cellular retinol-binding protein. J Cell Physiol 173:36-43
27. Li E, Demmer LA, Sweetser DA, Ong DE, Gordon JI 1986 Rat cellular retinol-binding protein II: use of a cloned cDNA to define its primary structure, tissue-specific expression, and developmental regulation. Proc Natl Acad Sci USA 83:5779-5783
28. Levin MS, Li E, Ong DE, Gordon JI 1987 Comparison of the tissue-specific expression and developmental regulation of two closely linked rodent genes encoding cytosolic retinol-binding proteins. J Biol Chem 262:7118-7124
29. Lampron C, Rochette-Egly C, Gorry P, Dolle P, Mark M, Lufkin T, LeMeur M, Chambon P 1995 Mice deficient in cellular retinoic acid binding protein II (CRABPII) or in both CRABPI and CRABPII are essentially normal. Development 121:539-548
30. Noy N 2000 Retinoid-binding proteins: mediators of retinoid action. Biochem J 348:481-495
31. Rajan N, Kidd GL, Talmage DA, Blaner WS, Suhara A, Goodman DS 1991 Cellular retinoic acid-binding protein messenger RNA: levels in rat tissues and localization in rat testis. J Lipid Res 32:1195-1204
32. Zheng WL, Bucco RA, Schmitt MC, Wardlaw SA, Ong DE 1996 Localization of cellular retinoic acid-binding protein (CRABP) II and CRABP in developing rat testis. Endocrinology 137:5028-5035
33. Chambon P 1996 A decade of molecular biology of retinoic acid receptors. FASEB J 10:940-954
34. Kastner P, Mark M, Ghyselinck N, Krezel W, Dupe V, Grondona JM, Chambon P 1997 Genetic evidence that the retinoid signal is transduced by heterodimeric RXR/RAR functional units during mouse development. Development 124:313-326
35. Mark M, Chambon P 2003 Functions of RARs and RXRs in vivo: genetic dissection of the retinoid signalling pathway. Pure Appl Chem 75:1709-1732
36. Glass CK, Rosenfeld MG 2000 The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev 14:121-141
37. Laudet V, Gronemeyer H 2002 The nuclear receptor facts book. London: Academic Press
38. Benkoussa M, Brand C, Delmotte MH, Formstecher P, Lefebvre P 2002 Retinoic acid receptors inhibit AP1 activation by regulating extracellular signal-regulated kinase and CBP recruitment to an AP1-responsive promoter. Mol Cell Biol 22:4522-4534
39. Kastner P, Mark M, Leid M, Gansmuller A, Chin W, Grondona JM, Decimo D, Krezel W, Dierich A, Chambon P 1996 Abnormal spermatogenesis in RXRβ mutant mice. Genes Dev 10:80-92
40. Akmal KM, Dufour JM, Kim KH 1997 Retinoic acid receptor-α gene expression in the rat testis: potential role during the prophase of meiosis and in the transition from round to elongating spermatids. Biol Reprod 56:549-556
41. Gaemers IC, van Pelt AM, van der Saag PT, Hoogerbrugge JW, Themmen AP, de Rooij DG 1998 Differential expression pattern of retinoid X receptors in adult murine testicular cells implies varying roles for these receptors in spermatogenesis. Biol Reprod 58:1351-1356
42. Dufour JM, Kim KH 1999 Cellular and subcellular localization of six retinoid receptors in rat testis during postnatal development: identification of potential heterodimeric receptors. Biol Reprod 61:1300-1308
43. Boulogne B, Levacher C, Durand P, Habert R 1999 Retinoic acid receptors and retinoid X receptors in the rat testis during fetal and postnatal development: immunolocalization and implication in the control of the number of gonocytes. Biol Reprod 61:1548-1557
44. Chapellier B, Mark M, Garnier JM, LeMeur M, Chambon P, Ghyselinck NB 2002 A conditional floxed (loxP-flanked) allele for the retinoic acid receptor-α (RARα) gene. Genesis 32:87-90
45. Dufour JM, Vo MN, Bhattacharya N, Okita J, Okita R, Kim KH 2003 Peroxisome proliferators disrupt retinoic acid receptor-α signalling in the testis. Biol Reprod 68:1215-1224
46. Saper CB, Sawchenko PE 2003 Magic peptides, magic antibodies: guidelines for appropriate controls for immunohistochemistry. J Comp Neurol 465:161-163
47. Russell LD, Ettlin RA, Sinha Hikim AP, Clegg ED 1990 Histological and histopathological evaluation of the testis. Clearwater, FL: Cache River Press
48. Décimo D, Georges-Labouesse E, Dollé P 1995 In situ hybridization of nucleic acid probes to cellular RNA. In: Hames BD, Higgins S, eds. Gene probes 2: a practical approach. Oxford, UK: Oxford University Press; 183-210
49. De Block M, Debrouwer D 1993 RNA-RNA in situ hybridization using digoxigenin-labeled probes: the use of high-molecular-weight polyvinyl alcohol in the alkaline phosphatase indoxyl-nitroblue tetrazolium reaction. Anal Biochem 215:86-89
50. Lufkin T, Lohnes D, Mark M, Dierich A, Gorry P, Gaub MP, LeMeur M, Chambon P 1993 High postnatal lethality and testis degeneration in retinoic acid receptor-α mutant mice. Proc Natl Acad Sci USA 90:7225-7229
51. Schnütgen F, Doerflinger N, Calleja C, Wendling O, Chambon P, Ghyselinck NB 2003 A directional strategy for monitoring Cre-mediated recombination at the cellular level in the mouse. Nat Biotechnol 21:562-565
52. Chapellier B, Mark M, Messaddeq N, Calleja C, Warot X, Brocard J, Gerard C, Li M, Metzger D, Ghyselinck NB, Chambon P 2002 Physiological and retinoid-induced proliferations of epidermis basal keratinocytes are differently controlled. EMBO J 21:3402-3413
53. Ghyselinck NB, Dupe V, Dierich A, Messaddeq N, Garnier JM, Rochette-Egly C, Chambon P, Mark M 1997 Role of the retinoic acid receptor-β(RARβ) during mouse development. Int J Dev Biol 41:425-447
54. Krezel W, Kastner P, Chambon P 1999 Differential expression of retinoid receptors in the adult mouse central nervous system. Neuroscience 89:1291-1300
55. Bellvé AR, Cavicchia JC, Millette CF, O'Brien DA, Bhatnagar YM, Dym M 1977 Spermatogenic cells of the prepubertal mouse. Isolation and morphological characterization. J Cell Biol 74:68-85
56. Wake K, Motomatsu K, Senoo H, Masuda A, Adachi E 1986 Improved Kupffer's gold chloride method for demonstrating the stellate cells storing retinol (vitamin A) in the liver and extrahepatic organs of vertebrates. Stain Technol 61:193-200
57. Ruiz A, Winston A, Lim YH, Gilbert BA, Rando RR, Bok D 1999 Molecular and biochemical characterization of lecithin retinol acyltransferase. J Biol Chem 274:3834-3841
58. Yost RW, Harrison EH, Ross AC 1988 Esterification by rat liver microsomes of retinol bound to cellular retinol-binding protein. J Biol Chem 263:18693-18701
59. Herr FM, Ong DE 1992 Differential interaction of lecithin-retinol acyltransferase with cellular retinol binding proteins. Biochemistry 31:6748-6755
60. Schmitt MC, Ong DE 1993 Expression of cellular retinol-binding protein and lecithin-retinol acyltransferase in developing rat testis. Biol Reprod 49:972-979
61. Londos C, Brasaemle DL, Schultz CJ, Segrest JP, Kimmel AR 1999 Perilipins, ADRP, and other proteins that associate with intracellular neutral lipid droplets in animal cells. Semin Cell Dev Biol 10:51-58
62. Mascrez B, Ghyselinck NB, Watanabe M, Annicotte JS, Chambon P, Auwerx J, Mark M 2004 Ligand-dependent contribution of RXRβ to cholesterol homeostasis in Sertoli cells. EMBO Rep 5:285-290
63. Imamura M, Inoguchi T, Ikuyama S, Taniguchi S, Kobayashi K, Nakashima N, Nawata H 2002 ADRP stimulates lipid accumulation and lipid droplet formation in murine fibroblasts. Am J Physiol Endocrinol Metab 283:775-783
64. -/- mutant mice are viable. Proc Natl Acad Sci USA 93:9010-9014
65. Fan X, Molotkov A, Manabe S, Donmoyer CM, Deltour L, Foglio MH, Cuenca AE, Blaner WS, Lipton SA, Duester G 2003 Targeted disruption of Aldh1a1 (Raldh1) provides evidence for a complex mechanism of retinoic acid synthesis in the developing retina. Mol Cell Biol 23:4637-4648
66. Dupé V, Matt N, Garnier JM, Chambon P, Mark M, Ghyselinck NB 2003 A newborn lethal defect due to inactivation of retinaldehyde dehydrogenase type 3 is prevented by maternal retinoic acid treatment. Proc Natl Acad Sci USA 100:14036-14041
67. Lohnes D, Kastner P, Dierich A, Mark M, LeMeur M, Chambon P 1993 Function of retinoic acid receptor-γ in the mouse. Cell 73:643-658
68. Eddy EM, Washburn TF, Bunch DO, Goulding EH, Gladen BC, Lubahn DB, Korach KS 1996 Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology 137:4796-4805
69. Yashiro K, Zhao X, Uehara M, Yamashita K, Nishijima M, Nishino J, Saijoh Y, Sakai Y, Hamada H 2004 Regulation of retinoic acid distribution is required for proximodistal patterning and outgrowth of the developing mouse limb. Dev Cell 6:411-422
70. Chung SS, Wang X, Wolgemuth DJ 2005 Male sterility in mice lacking retinoic acid receptor-α involves specific abnormalities in spermiogenesis. Differentiation 73:188-198
71. Schultz R, Penttila TL, Parvinen M, Persson H, Hokfelt T, Pelto-Huikko M 1995 Expression of immediate early genes in tubular cells of rat testis. Biol Reprod 52:1215-1226
72. Metzger D, Chambon P 2001 Site- and time-specific gene targeting in the mouse. Methods 24:71-80
73. Lécureuil C, Fontaine I, Crepieux P, Guillou F 2002 Sertoli and granulosa cell-specific Cre recombinase activity in transgenic mice. Genesis 33:114-118
74. Weber P, Cammas F, Gerard C, Metzger D, Chambon P, Losson R, Mark M 2002 Germ cell expression of the transcriptional co-repressor TIF1β is required for the maintenance of spermatogenesis in the mouse. Development 129:2329-2337
75. Haselbeck RJ, Hoffmann I, Duester G 1999 Distinct functions for Aldh1 and Raldh2 in the control of ligand production for embryonic retinoid signalling pathways. Dev Genet 25:353-364
76. Gaemers IC, van Pelt AM, van der Saag PT, de Rooij DG 1996 All-trans-4-oxo-retinoic acid: a potent inducer of in vivo proliferation of growth-arrested A spermatogonia in the vitamin A-deficient mouse testis. Endocrinology 137:479-485
77. Yamanushi T, Igarashi O 1995 The mobilization and tissue distribution of β-carotene in the rat by the venous injection method. J Nutr Sci Vitaminol (Tokyo) 41:169-177
78. Abu-Abed S, MacLean G, Fraulob V, Chambon P, Petkovich M, Dolle P 2002 Differential expression of the retinoic acid-metabolizing enzymes CYP26A1 and CYP26B1 during murine organogenesis. Mech Dev 110:173-177
79. Rajguru SU, Kang YH, Ahluwalia BS 1982 Localization of retinol (vitamin A) in rat testes. J Nutr 112:1881-1891
80. Shingleton JL, Skinner MK, Ong DE 1989 Retinol esterification in Sertoli cells by lecithin-retinol acyltransferase. Biochemistry 28:9647-9653
81. Batten ML, Imanishi Y, Maeda T, Tu DC, Moise AR, Bronson D, Possin D, Van Gelder RN, Baehr W, Palczewski K 2004 Lecithin-retinol acyltransferase is essential for accumulation of all-trans-retinyl esters in the eye and in the liver. J Biol Chem 279:10422-10432
82. Chaudhary LR, Nelson EC 1987 Some properties and subcellular distribution of acyl-coenzyme A: retinol acyltransferase activity in rat testes. Biochim Biophys Acta 917:24-32